Evolvability is a selectable trait
Abstract
Concomitant with the evolution of biological diversity must have been the evolution of mechanisms that facilitate evolution, because of the essentially infinite complexity of protein sequence space. We describe how evolvability can be an object of Darwinian selection, emphasizing the collective nature of the process. We quantify our theory with computer simulations of protein evolution. These simulations demonstrate that rapid or dramatic environmental change leads to selection for greater evolvability. The selective pressure for large-scale genetic moves such as DNA exchange becomes increasingly strong as the environmental conditions become more uncertain. Our results demonstrate that evolvability is a selectable trait and allow for the explanation of a large body of experimental results.
Acknowledgments
We thank Kevin R. Foster for a careful reading of the manuscript. This research is supported by the National Institutes of Health.
References
1
Gould, S. J. (1983) Hen's Teeth and Horse's Toes (Norton, New York).
2
Kirschner, M. & Gerhart, J. (1998) Proc. Natl. Acad. Sci. USA 95, 8420–8427.
3
Dawkins, R. (1989) in Artificial Life, ed. Langton, C. G. (Addison–Wesley, New York), pp. 201–220.
4
Radman, M., Matic, I. & Taddei, F. (1999) Ann. N.Y. Acad. Sci. 870, 146–155.
5
Chicurel, M. (2001) Science 292, 1824–1827.
6
Partridge, L. & Barton, N. H. (2000) Nature 407, 457–458.
7
Kidwell, M. G. (1997) Proc. Natl. Acad. Sci. USA 94, 7704–7711.
8
Shapiro, J. A. (1997) Trends Genet. 13, 98–104.
9
Barton, N. H. & Charlesworth, B. (1998) Science 281, 1986–1990.
10
Fedoroff, N. (2000) Proc. Natl. Acad. Sci. USA 97, 7002–7007.
11
Shapiro, J. A. (2002) J. Biol. Phys. 28, 745–764.
12
Shapiro, J. A. (2002) Ann. N.Y. Acad. Sci. 981, 111–134.
13
Storb, U. (2001) Nat. Immunol. 2, 484–485.
14
Plotkin, J. B. & Dushoff, J. (2003) Proc. Natl. Acad. Sci. USA 100, 7152–7157.
15
Caporale, L. H. (2003) Am. Sci. 91, 234–241.
16
Kepler, T. B. (1997) Mol. Biol. Evol. 14, 637–643.
17
Friedberg, E. C., Feaver, W. F. & Gerlach, V. L. (2000) Proc. Natl. Acad. Sci. USA 97, 5681–5683.
18
Freire, E. (2002) Nat. Biotechnol. 20, 15–16.
19
Kepler, T. B. & Perelson, A. S. (1998) Proc. Natl. Acad. Sci. USA 95, 11514–11519.
20
Rosenberg, S. M. (2001) Nat. Rev. Genet. 2, 504–515.
21
Pepper, J. W. (2003) BioSystems 69, 115–126.
22
Colegrave, N. (2002) Nature 420, 664–666.
23
Frank, S. A. (2002) Immunology and Evolution of Infectious Disease (Princeton Univ. Press, Princeton).
24
Wagner, G. P. & Altenberg, L. (1996) Evolution (Lawrence, Kans.) 50, 967–976.
25
Lenski, R. E., Ofria, C., Pennock, R. T. & Adami, C. (2003) Nature 423, 139–144.
26
Blasio, F. V. D. (1999) Phys. Rev. E 60, 5912–5917.
27
Travis, J. M. J. & Travis, E. R. (2002) Proc. R. Soc. London Ser. B 269, 591–597.
28
Siegal, M. L. & Bergman, A. (2002) Proc. Natl. Acad. Sci. USA 99, 10528–10532.
29
Bergman, A. & Siegal, M. L. (2003) Nature 424, 549–552.
30
Shapiro, J. A. (1992) Genetica 86, 99–111.
31
Lawrence, J. G. (1997) Trends Microbiol. 5, 355–359.
32
Zhang, Y.-X., Perry, K., Vinci, V. A., Powell, K., Stemmer, W. P. C. & del Cardayre, S. B. (2002) Nature 415, 644–646.
33
Pennisi, E. (1998) Science 281, 1131–1134.
34
Gilbert, W. (1978) Nature 271, 501.
35
Gilbert, W., DeSouza, S. J. & Long, M. (1997) Proc. Natl. Acad. Sci. USA 94, 7698–7703.
36
Duret, L., Marais, G. & Biemont, C. (2000) Genetics 156, 1661–1669.
37
Lonnig, W.-E. & Saedler, H. (2002) Annu. Rev. Genet. 36, 389–410.
38
Levin, B. R. & Bergstrom, C. T. (2000) Proc. Natl. Acad. Sci. USA 97, 6981–6985.
39
Doolittle, W. F. (2000) Sci. Am. 282 (2), 90–95.
40
Stemmer, W. P. C. (1994) Nature 370, 389–391.
41
Crameri, A., Raillard, S. A., Bermudez, E. & Stemmer, W. P. C. (1998) Nature 391, 288–291.
42
Zhang, J.-H., Dawes, G. & Stemmer, W. P. C. (1997) Proc. Natl. Acad. Sci. USA 94, 4504–4509.
43
Moore, J. C., Jin, H.-M., Kuchner, O. & Arnold, F. H. (1997) J. Mol. Evol. 272, 336–347.
44
Lutz, S. & Benkovic, S. J. (2000) Curr. Opin. Biotechnol. 11, 319–324.
45
Clarke, B. C. (1979) Proc. R. Soc. London Ser. B 205, 453–474.
46
Dawkins, R. & Krebs, J. R. (1979) Proc. R. Soc. London Ser. B 205, 489–512.
47
Gould, S. J. & Lewontin, R. C. (1979) Proc. R. Soc. London Ser. B 205, 581–598.
48
Gillespie, J. H. (1991) The Causes of Molecular Evolution (Oxford Univ. Press, Oxford).
49
Frank, S. A. & Slatkin, M. (1990) Am. Nat. 136, 244–260.
50
Smith, J. M. (1979) Proc. R. Soc. London Ser. B 205, 475–488.
51
Smith, J. M. (1982) Evolution and the Theory of Games (Cambridge Univ. Press, Cambridge, U.K.).
52
Sasaki, A. & Ellner, S. (1995) Evolution (Lawrence, Kans.) 49, 337–350.
53
Sato, K., Ito, Y., Yomo, T. & Kaneko, K. (2003) Proc. Natl. Acad. Sci. USA 100, 14086–14090.
54
Bogarad, L. D. & Deem, M. W. (1999) Proc. Natl. Acad. Sci. USA 96, 2591–2595.
55
Kauffman, S. & Levin, S. (1987) J. Theor. Biol. 128, 11–45.
56
Kauffman, S. A. (1993) The Origins of Order (Oxford Univ. Press, New York).
57
Kauffman, S. A. & MacReady, W. G. (1995) J. Theor. Biol. 173, 427–440.
58
Perelson, A. S. & Macken, C. A. (1995) Proc. Natl. Acad. Sci. USA 92, 9657–9661.
59
Deem, M. W. & Lee, H. Y. (2003) Phys. Rev. Lett. 91, 068101.
60
Michod, R. E. & Levin, B. R., eds. (1988) The Evolution of Sex (Sinauer, Sunderland, MA).
61
Chandrasekhar, S. (1943) Rev. Mod. Phys. 15, 1–89.
62
Aguilar, A., Roemer, G., Debenham, S., Binns, M., Garcelon, D. & Wayne, R. K. (2004) Proc. Natl. Acad. Sci. USA 101, 3490–3494.
63
Zhu, T. F., Korber, B. T., Nahmias, A. J., Hooper, E., Sharp, P. M. & Ho, D. D. (1998) Nature 391, 594–597.
64
Gao, F., Bailes, E., Robertson, D. L., Chen, Y. L., Rodenburg, C. M., Michael, S. F., Cummins, L. B., Arthur, L. O., Peeters, M., Shaw, G. M., et al. (1999) Nature 397, 436–441.
65
Lederberg, J., Shope, R. E. & S. C. Oaks, J., eds. (1992) Emerging Infections: Microbial Threats to Health in the United States (Natl. Acad. Press, Washington, DC).
66
Levy, D. N., Aldrovandi, G. M., Kutsch, O. & Shaw, G. M. (2004) Proc. Natl. Acad. Sci. USA 101, 4204–4209.
67
Tan, T., Bogarad, L. D. & Deem, M. W. (2004) J. Mol. Evol., in press.
68
Elena, S. F. & Lenski, R. E. (2003) Nat. Rev. Genet. 4, 457–469.
69
Reboud, X. & Bell, G. (1997) Heredity 78, 507–514.
70
Bennett, A. F. & Lenski, R. E. (1993) Evolution (Lawrence, Kans.) 47, 1–12.
71
Leroi, A. M., Lenski, R. E. & Bennett, A. F. (1994) Evolution (Lawrence, Kans.) 48, 1222–1229.
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Copyright © 2004, The National Academy of Sciences. Freely available online through the PNAS open access option.
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Received: April 19, 2004
Published online: August 2, 2004
Published in issue: August 10, 2004
Acknowledgments
We thank Kevin R. Foster for a careful reading of the manuscript. This research is supported by the National Institutes of Health.
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Evolvability is a selectable trait, Proc. Natl. Acad. Sci. U.S.A.
101 (32) 11531-11536,
https://doi.org/10.1073/pnas.0404656101
(2004).
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